CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2010 5, No. 043 Review Rice hoja blanca: a complex plant–virus–vector pathosystem F.J. Morales* and P.R. Jennings

Address: International Centre for Tropical Agriculture, AA 6713, Cali, Colombia.

*Correspondence: F.J. Morales. E-mail: [email protected]

Received: 30 April 2010 Accepted: 24 June 2010

doi: 10.1079/PAVSNNR20105043

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews

g CAB International 2009 (Online ISSN 1749-8848)

Abstract

Rice hoja blanca (RHB; white leaf) devastated rice (Oryza sativa) plantings in tropical America for half a century, before scientists could either identify its causal agent or understand the nature of its cyclical epidemics. The association of the planthopper Tagosodes orizicolus with RHB outbreaks, 20 years after its emergence in South America, suggested the existence of a viral pathogen. However, T. orizicolus could also cause severe direct feeding damage (hopperburn) to rice in the absence of hoja blanca, and breeders promptly realized that the genetic basis of resistance to these problems was different. Furthermore, it was observed that the causal agent of RHB could only be trans- mitted by a relatively low proportion of the individuals in any given population of T. orizicolus and that the pathogen was transovarially transmitted to the progeny of the planthopper vectors, affecting their normal biology. An international rice germplasm screening effort was initiated in the late 1950s to identify sources of resistance against RHB and the direct feeding damage caused by T. orizicolus, making better progress in the development of hopperburn-resistant than for hoja- blanca-resistant rice lines. In the 1980s, the identification of a novel virus as the causal agent of RHB, and genetic studies on the interaction of this virus with its planthopper vector, confirmed previous studies on the pathogenic nature of the virus to T. orizicolus and helped explain the cyclical nature of RHB epidemics. This disease is best controlled by hybridization of susceptible indica and resistant japonica rice genotypes and the adoption of integrated disease control practices.

Keywords: Rice hoja blanca (RHB) virus, Oryza sativa, Tagosodes orizicolus, Sogata, Tenuivirus, Echinochloa colona

Review Methodology: We searched CAB Abstracts,CIAT’s Rice Program Annual Reports and personal research files.

Introduction rice plantings in Brazil, Belize, Colombia, Costa Rica, Cuba, Dominican Republic, El Salvador, Ecuador, Guatemala, Rice ‘hoja blanca’ (white leaf) is one of the most complex, Guyana, Honduras, Mexico, Nicaragua, Panama, Peru, puzzling, challenging and, all the same, interesting patho- Puerto Rico, Surinam, USA and Venezuela [4]. Besides its systems encountered in the field of plant virology. Rice notable spatial dissemination capacity, the main concern hoja blanca (RHB) gained notoriety in the mid-1950s, of rice growers and agricultural scientists was the sig- when it emerged in the state of Florida, threatening nificant yield losses (25–75%) that this disease could rice production in the southeastern USA [1]. However, induce in susceptible rice cultivars, as a result of seedling RHB was first observed in rice fields of the Cauca Valley death, reduced photosynthetic capacity, plant dwarfing AQ1 department of Colombia, around 1935 [2]. Two decades and panicle sterility [3, 5, 6]. later, RHB was present in the neighbouring countries The broad geographic distribution of RHB and its of Panama, Venezuela and Costa Rica, and had crossed capacity to breach extensive natural barriers, such as the the Caribbean Sea to reach Cuba and the Florida penin- Caribbean sea, were explained in 1957 when preliminary sula [3]. Within a decade, RHB was widely distributed investigations conducted in Cuba [7, 8] and Venezuela [9] throughout tropical and subtropical America, affecting associated the incidence of RHB with the presence of the

http://www.cabi.org/cabreviews 2 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources planthopper (Homoptera: Delphacidae) Sogata orizicola name (white leaf); stunting, panicle sterility and/or plant (Muir) in RHB-affected rice fields. Further testing of these death. Affected plants may show the disease symptoms in suspected vectors led to the conclusion that only Soga- some tillers, while other tillers remain symptomless. The todes orizicola was the vector of the causal agent of RHB panicles of diseased tillers are shorter and malformed, [10, 11]. In 1993, the taxonomy of this planthopper including the lemma and palea of florets that dry out and species was further reviewed to include it in the genus show a brownish discoloration [20]. Although disease Tagosodes, species orizicolus [12]. Rice planthoppers are incidence and severity were variable, some affected rice known long-distance fliers, capable of covering distances fields in the Cauca Valley had to be ploughed under in in excess of 1000 km without alighting [13]. Planthoppers 1958. Varieties such as Bluebonnet 50, Century Patna 231, are also proven vectors of different plant viruses affecting Early Prolific, Fortuna, Guayaquil, Lady Wright, Nato, plant species of the Gramineae, including rice, which Rexoro, Santa Maria and Zenith proved highly susceptible, suggested that RHB was caused by a virus [2, 14]. How- as well as many of the 2200 lines of the world collection of ever, the aetiology and epidemiology of RHB had to wait the US Department of Agriculture of the USA evaluated in almost half a century to be elucidated. Colombia, Cuba and Venezuela. A second group of 1725 One of the most puzzling characteristics of the RHB lines from the USA and FAO genebanks was also screened pathosystem is its erratic, ‘cyclical’ epidemic behaviour. in Cuba and Colombia. Of these field evaluations, about RHB caused significant (25–50%) yield losses in 1957– 400 resistant rice genotypes were identified in these 1964, just to fade away in the following 15 years (1965– collections, mainly belonging to short-grain japonica types 1980), and then re-emerge in full force from 1981 until from Japan, China, Korea and Taiwan [5, 6]. The main 1984 [1, 3, 15] (Peter R. Jennings, 2010, unpublished data). sources of resistance selected from the US collection The last outbreak of RHB in Colombia took place in were Gulfrose and Lacrosse (subtropical japonicas). 1996–1999. Considering that no hoja-blanca-resistant rice Disease incidence and severity seemed to depend on the varieties were available during those years, it became time of infection: with early infection (1–3 leaf stage) evident that the cyclical nature of the RHB epidemics resulting in higher incidence and disease severity [2, 21]. was more likely determined by the interaction between Based on these field evaluations conducted in 1956 the pathogen and the insect vector Tagosodes orizicolus and 1957, a breeding project was initiated in Palmira [7, 16, 17]. (Colombia) to transfer the resistance found in the japonica grain types to the susceptible long-grain, indica varieties preferred in tropical America. The Plant Host

Rice (Oryza sativa L.) is the second most extensive food The Insect Vector crop grown in the world (c. 159 million ha) after wheat and is the main food crop grown in the tropics. Half of the T. orizicolus (Muir), commonly referred to as ‘sogata’, has world’s population (over 3 billion people) depends on been consistently shown to be the vector of the causal rice, particularly in Asia, where annual per capita rice agent of RHB [7, 9, 10, 11]. A related planthopper species, consumption may be as high as 170 kg in countries such as T. cubanus, common in rice fields, can be experimentally Vietnam. Asia produces almost 90% of all the rice culti- forced to transmit the RHB agent from rice to its pre- vated in the world (141 million ha), mainly China and ferred wild host, Echinochloa colona (L.) Link, and from India, where rice domestication and cultivation seems to E. colona to E. colona under natural field conditions [22]. have started over 5000 years ago. Africa cultivates ap- The species T. orizicolus and T. cubanus (Homoptera: proximately 9.5 million ha, and the Americas 6.8 million ha Delphacidae) are restricted to tropical and subtropical of rice. Nevertheless, over half a billion people consume America, although T. cubanus has been reported from up to 43 kg of rice per year/per capita in Latin America West Africa as well [23]. However, the genus Tagosodes and the Caribbean, which demonstrates the importance appears to be of Asian origin [23, 24], as is the case with of this grain crop in the regional diet [18]. its main hosts, rice and E. colona [25]. Unlike the complex phytosanitary situation of rice in T. orizicolus was originally described by Muir [26] as Asia, where several viruses affect this grain crop, RHB was Sogata orizicola in 1926 from specimens collected in British the only viral disease of rice in the Americas until a new Guiana. The name Sogata brasilensis or brazilensis has also virus, Rice stripe necrosis virus (RSNV), emerged in South appeared in the early literature. In 1963, Fennah [27] America in 1991 [19]. However, the economic impor- changed the genus to Sogatodes, and Ishihara and Nasu tance of RSNV has been so far relatively negligible. On the [28] changed the spelling of the species name from orizi- contrary, the pathogenicity and severity of the causal cola to oryzicola. Finally, as mentioned above, the name of agent of RHB were apparent from the time this disease this planthopper species was changed to T. orizicolus in the was originally observed in the Cauca valley of Colombia. 1990s [12, 29]. T. cubanus was first described by Crawford Affected rice plants showed the characteristic yellowish, [30] as Dicranotropis cubanus from Cuban specimens. chlorotic stripes that often coalesce to give RHB its Other names used in the past to describe this species

http://www.cabi.org/cabreviews F.J. Morales and P.R. Jennings 3 were: Megamelus flavolineatus, Delphacodes pallividitta and virus were made at an advanced virology laboratory Chloriona (Sogatella) panda [23]. T. orizicolus and T. cubanus (Instituto Venezolano de Investigaciones Cientificas, IVIC), are similar in size (2–5 mm long), but T. cubanus tends to in Caracas, Venezuela. The RHB investigation conducted be smaller. Females are characteristically larger and more at about 1968 resulted in the isolation of isometric robust than males, and their body colour varies from dark (round-like) particles (42 nm in diameter) from RHB- to light brown, with males being darker than females. Both affected rice plants [34]. However, electron microscopy alatae and brachypterous individuals are found in any studies conducted in Japan a year later [35] revealed the given population of Tagosodes spp., with brachyptery being presence of filamentous particles (8–10 mm in diameter more frequent in T. orizicolus and females of both species. and about 2000 nm in length) in the cells of infected rice T. orizicolus requires moderately high temperatures and plants and sogata vectors, similar to those reported for high humidity (about 27C and >80% RH, respectively) for closteroviruses (e.g. Citrus tristeza virus). A Brazilian study normal development. Eggs are laid in a cluster in the yielded similar results upon examination of the infected midrib of the rice leaf blade or in the leaf sheath, usually in cells of the weed E. colona [36], which often shows hoja multiples of seven. Eggs are about 0.7 mm long, white, and blanca symptoms in RHB-affected rice fields. Adding to are very sensitive to desiccation. Incubation periods vary the discrepancy of these previous reports, a new inves- according to temperature with a minimum of a week tigation on the aetiology of RHB, conducted in Cuba [37], at 27C and a maximum of two weeks at 18C. Each concluded that the causal agent was not a virus, but a nymphal stadium takes 3–7 days and 2–3 weeks for phytoplasma (bacteria-like micro-organism of the class complete nymphal development. The first instar nymph Mollicutes). (0.5 mm long) emerges on the adaxial surface of the leaf The final attempt at isolating and characterizing the and starts feeding within 24 h. Second instar nymphs are RHB pathogen began in the early 1980s, taking advantage 1 mm long and subsequent inmatures belonging to the of new disease outbreaks in CICA 8 and IR 22 rice fields third, fourth and fifth instars grow up to an average size located in the department of Tolima, Colombia. The of 2.5 mm. Adult females are larger than males and live infected plant extracts were processed following new longer than males within the 24–36 longevity range purification protocols based on self-forming caesium described for T. orizicolus. Mating may start two days after chloride and caesium sulphate density gradients. Light- the final moult, and mated females begin oviposition three scattering bands were formed in both caesium salts when to five days later, laying about 10 eggs/day for a total diseased rice plant extracts were centrifuged, but not average of 160 eggs. Virgin females may lay fewer eggs when extracts from healthy rice plants were used. The (about half as many), but parthenogenesis has not been electron microscopy of the recovered bands obtained reported for these species [14]. after 19 h of centrifugation revealed the presence of very T. orizicolus is also a direct pest of rice, being capable of fine filamentous particles, approximately 3 nm in diameter causing significant feeding damage (hopperburn) and yield and of variable length, with a tightly spiralled configura- losses in rice varieties that attract and support large tion. These particles had the characteristic ultraviolet populations of this planthopper species. Genetic resis- absorption spectrum of a nucleo-protein when assayed tance to the direct damage of sogata is available and by UV spectrophotometry (A260/280 nm ratio of 1.4+0.02). widely used in rice improvement programmes, but the The purified RHB preparations produced a predominant genetic basis of this resistance is different from the protein of 34103 Da and a minor protein of 17.5103 genetics of resistance to RHB virus (RHBV) [31]. Da. An antiserum prepared with these purified suspen- sions specifically detected the causal agent of RHB in diseased rice plants, but did not react with extracts from The RHB Pathogen healthy rice plants [33]. These findings led to the con- clusion that the RHB causal agent belonged to a new Although, following the demonstration in 1957 that a group of plant viruses not yet recognized by the Inter- planthopper (sogata) was associated with RHB [7, 9] and national Committee on Taxonomy of Viruses (ICTV), the observation that RHB symptoms were similar to together with two other new viruses affecting rice in Asia those of rice stripe in Japan [32], the causal agent was (Rice stripe virus, RSV), and maize in North America (Maize assumed to be a virus, its isolation and characterization stripe virus, MspV) [38, 39]. These viruses were accepted took almost 50 years from the original report of RHB and classified by the ICTV in 1995 and finally placed in the in Colombia, in 1935 [4, 33]. The reasons for this long new Tenuivirus genus [40]. period of fruitless research on the aetiology of RHB were Tenuiviruses have a thin (3–8 nm in diameter) fila- multiple: the difficulty of working with viruses at a time mentous shape and variable lengths determined by the when plant virology was still developing as a science; the size of the RNA molecules they contain, and the different lack of the advanced molecular techniques we have today structural forms they adopt (spiral, circular or branched at our disposal; and the fact that RHBV belonged to a particles). These particles are nucleoproteins without an group of plant viruses not yet known to plant virologists envelope. Purified tenuivirus particles can be separated prior to 1980. The first attempts to isolate the causal into four or five components by sucrose density gradient

http://www.cabi.org/cabreviews 4 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources centrifugation, but form only one component when and survival of its insect vector, the planthopper T. orizi- centrifuged in caesium salts, to a buoyant density of colus. This planthopper is currently distributed throughout 1.28 g/cm3. The ssRNA genome of tenuiviruses consists of tropical America, and it has been able to survive in some four or more segments. The RHBV genome has four subtropical regions of the Americas, such as southern visible ssRNA species [41]. The 9 kb RNA-1 is generally USA [14] and northeast Argentina [47]. However, RHBV of negative polarity, whereas the remaining RNAs 2–4 is not currently found in these subtropical areas. T. orizi- have an ambisense translation strategy. The nucleocapsid colus requires high humidity and optimum average tem- protein of RHBV has a size of 34 kDa [33] and is encoded peratures in the 24–28C range. The eggs are extremely by the 50 -proximal region of the virion-complementary sensitive to low relative humidity conditions, but the sense strand of RNA-3. The virion-sense RNA-4 mole- conditions found in irrigated rice fields or rain-fed rice AQ2 cule encodes a major non-structural protein (NCP)of fields in the tropics are quite favourable for the repro- 17.5 kDa, which accumulates in RHB-infected rice plants duction of T. orizicolus. Under these conditions, a new [33, 41]. There is no evidence of significant pathogenic cycle from oviposition to the adult stage can be com- variability or development of more pathogenic RHBV pleted in less than a month [14]. T. orizicolus survives well strains in Latin America. For instance, a comparative study on certain rice varieties, such as Bluebonnet 50, CICA-8, of Colombian and Costa Rican isolates of RHBV yielded Metica-1, Oryzica-1, Arkrose, Nato and Gulfrose, but not nucleotide sequence homologies between 91 and 98.9% on all rice genotypes (e.g. Nilo 1, Zayas Bayan and Dima); for the coding and non-coding RNA-3 and RNA-4 com- as well as on some related species, such as O. perennis, ponents of the selected isolates [42]. but not on O. barthii, O. glaberrima, O. grandiglumis and O. latifolia. Several cultivated and wild grasses have been reported to be experimental or suspected hosts of both Relationships to other Tenuiviruses the virus and the planthopper vector. Wheat (Triticum aestivum L.), barley (Hordeum vulgare L.), oats (Avena sativa The genus Tenuivirus includes two additional viruses of L.) and rye (Secale cereale (L.) Bieb.) have been shown rice: RSV and Rice grassy stunt virus (RGSV) in Asia; MspV, to be natural or experimental hosts of RHBV [48–50]. of worldwide distribution; and two neotropical viruses of However, these alternate hosts do not seem to act as weeds, related to RHBV: Echinochloa hoja blanca virus virus reservoirs for transmission to occur back to rice (EHBV) and Urochloa hoja blanca virus (UHBV). Tentative [22], even though some of these species are highly sus- tenuiviruses (not yet accepted by the ICTV) include: ceptible to RHBV [15]. Many wild grasses have been another rice virus, namely Rice wilted stunt virus, Maize observed to show hoja blanca symptoms in RHB-affected yellow stripe virus and at least four tenuiviruses isolated regions. E. colona seems to be the most frequent weed from wheat (ICTV). At the molecular level, RHBV is more present in rice fields affected by RHBV, and may have closely related to EHBV and UHBV than to RSV, RGSV or been the original source of RHBV [3], but this weed has MSpV [43]. RHBV is not serologically related to the Asian been shown to be a dead-end host of the virus in ex- rice tenuiviruses RSV or RGSV. perimental RHBV transmission assays [22]. Other weeds RHBV is most closely related to EHBV, to the extent reported to exhibit hoja blanca symptoms are Brachiaria that their capsid and non-capsid proteins are antigenically plantaginea, Echinochloa crus-galli, E. walteri, Panicum fasci- related and very similar. These two viruses occupy the culatum, P. capillare, Paspalum sp. and Rottboellia exaltata same agro-ecological zones and usually co-exist in most [11, 48, 51], but the causal agents have not been shown to rice fields where RHB is a problem. However, RHBV and be RHBV. EHBV have different vectors (T. orizicolus and T. cubanus, Nymphs, females and young males of T. orizicolus are respectively), even though T. cubanus can be forced usually located on the lower portion of the plant, whereas to transmit RHBV under experimental conditions [21], adult males may be found higher up on the infested rice which explains why RHBV and EHBV are consistently plants. Hence, trapping sogata with nets may not reveal found to cause single infections in either rice or E. colona, the real composition of the planthopper population. In respectively. At the molecular level, EHBV has a smaller Latin America and the Caribbean, where rice is grown all RNA-4 than RHBV, and their nucleotide sequence identity year round, T. orizicolus does not seem to have the need only amounts to 80–85% and 46–53% in the coding and to migrate long distances [52], as rice planthoppers in non-coding regions, respectively [44, 45]. Consequently, temperate regions of Asia do [53]. Therefore, short dis- RHBV and EHBV are currently considered as distinct tance dispersal into rice fields and within-field dispersal of species of the genus Tenuivirus [43, 46]. sogata populations may be the norm soon after seedling emergence, and as long as the plant remains in its vege- tative stage. Upon crop flowering, the winged individuals Epidemiology of RHBV tend to leave the plants in search of younger rice plant- ings. With a life cycle of about a month, 2–3 generations The geographic distribution of RHBV is determined by the may develop in a rice field. Double cropping allows a environmental conditions that favour the reproduction significant build up of the sogata vector in rice fields [14].

http://www.cabi.org/cabreviews F.J. Morales and P.R. Jennings 5 RHBV is a circulative, propagative and transovarially Progenies from non-vector parents from lineages includ- transmitted virus in its insect vector, T. orizicolus. These ing at least one vector, segregated in a fashion consistent terms mean that a potential planthopper vector requires with the presence of a single recessive gene (r) controlling up to 12 h to acquire the virus from a systemically infected the ability to support RHBV replication in T. orizicolus.A rice plant, even though some individuals can acquire the strong maternal influence on the ability of the planthopper virus in less than an hour, with an optimum acquisition to support virus replication was observed in this investi- feeding time of 8 h [16], and then requires a minimum of gation. Active female vectors transmitted RHBV transo- a week to a month to complete its incubation period varially to their progeny regardless of the male parent, and inside the vector. During these acquisition and incubation these could transmit the virus to the susceptible test periods, the virus circulates from the sucking mouth parts plants. However, these individuals had a lower virus titre of the insect to its midgut, where it penetrates into the than those obtained from ELISA-positive parents, and they haemolymph, to finally reach the salivary glands in order could lose their ability to transmit RHBV to susceptible to be transmitted back into a healthy rice plant upon plants. feeding by nymphs, female and male adults for 3–7 h to The above investigation and the low percentage of infect at least 90% of the test plants [16, 21]. Considering RHBV vectors in any given population of T. orizicolus, even the short life span of the latter stage, adult males usually during an epidemic phase of the virus, show that the ability acquire the virus through the egg. Transovarial trans- of an individual sogata to support virus replication is under mission was first demonstrated by Acun˜a et al. [7]. Female genetic control. As mentioned before, the ability of the adults can acquire the virus during the nymphal stage RHBV to replicate in the planthopper and its deleterious because of their longer life span [3, 7, 9, 10, 11, 16, 35]. effects on its fecundity mean that RHBV is also a pathogen The ability of RHBV to reproduce in its insect vector of T. orizicolus. Thus, the dominant allele (R) that does not means that it does it at the expense of the bio-synthetic support multiplication of the virus protects the plant- capacity of the insect (as in a susceptible plant) and, hopper from the ill effects of the virus and prevents RHBV consequently, it can infect and induce deleterious effects transmission in rice fields. At this stage, the proportion of in its insect vector. This fact was demonstrated by vectors to non-vectors further diminishes, bringing about Jennings and Pineda [17], who showed that T. orizicolus a reduction in disease incidence and, hence, the end of vectors laid one-third as many eggs and hatched fewer an epidemic cycle. However, the recessive (r) gene that nymphs than did virus-free individuals. The life expectancy supports virus replication is maintained in homozygous or of nymphs and adults was also significantly reduced. The heterozygous form in the T. orizicolus population. authors associated the observation that only 5–15% of the It is also possible, as in the case of insects that develop individuals in a given sogata population can transmit the genetic resistance to insecticides or pathogens [56–58], virus in nature [50], with the deleterious effect of RHBV in that there is a ‘fitness cost’ [59] for the RHBV-resistant virus vectors, and the subsequent decline in the number individuals of T. orizicolus. That is, a trade-off in which of RHBV vectors at the end of a disease cycle. alleles conferring higher fitness in one environment (e.g. AQ3 The above hypothesis was investigated by Zeigler and presence of RHBV) reduce fitness in an alternative Morales [54], who studied the inheritance of the ability of environment (e.g. absence of RHBV), which may even- T. orizicolus to support replication of RHBV by following tually lead to an increase in the proportion of rr individuals the segregation of progeny derived from crosses between in the absence of the virus once an epidemic comes to an insects of known pedigree and virus transmission capacity. end. Be that as it may, either because of a gradual increase Evidence of RHBV replication inside the sogata individuals in the number of rr individuals derived from heterozygous allowed access to a virus source was investigated using the (Rr) resistant individuals or because of a genetic reversion immuno-enzymatic enzyme-linked immuno-sorbent assay to the original (optimal) fitness state in the absence of the (ELISA) method [55] adapted for this purpose. A post- pathogenic virus, the proportion of rr individuals capable acquisition period of 12 days was required before RHBV of supporting RHBV replication eventually increases, thus could be detected by ELISA in the sogata vectors, showing creating the conditions for a future RHB outbreak. The that this virus replicates in T. orizicolus. A minimum of 20 genetic control of RHBV transmission in T. orizicolus is also days was then required for the virus to be transmitted to demonstrated by the observation that highly viruliferous susceptible rice plants (Bluebonnet 50), that is, to com- sogata colonies produced by selected crosses between plete the virus incubation period. In these experiments, proven RHBV vectors eventually regress to populations individuals who supported RHBV replication, as deter- containing a reduced number of RHBV vectors, after the mined by ELISA, but who could not transmit RHBV before directed crosses are terminated [21, 60]. the incubation period (20–25 days) was completed, were considered ‘potential’ vectors. Non-vectors were identi- fied by their inability to transmit the virus at the end of its Genetic Resistance incubation period, and by their negative ELISA reaction. ‘Active’ vectors were those individuals who could trans- In 1956, a severe RHBV epidemic swept throughout mit the virus before the incubation period was completed. Central America, the Caribbean and tropical South

http://www.cabi.org/cabreviews 6 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources America. All rice varieties under cultivation at that time sogata causing massive crop damage through hopperburn. were highly virus- and sogata-susceptible and yield losses However, swollen sogata populations did not extend the were up to 100%. Crop losses were exclusively the result hoja blanca epidemic or incite a new one in subsequent of virus infection as farmers had not yet begun using years. After the RHBV epidemic ended in about 1964, and insecticides to control planthopper vectors. the mechanical damage caused by sogata became more In 1957, the Colombian Ministry of Agriculture req- important, RHBV resistance breeding ceased in all Latin uested assistance of the Colombian Agricultural Program America programmes except that of Peru, where the of the Rockefeller Foundation to create a national rice Amazonian locality of Bagua remained an intermittent hot research programme. The initial objective of the new spot for field selection of RHBV-resistant parents and breeding programme was to develop rice varieties with segregating populations in the following years [64] (Peter hoja blanca resistance. The USDA provided its germplasm Jennings, 2010, unpublished data). This change in crop collection, totalling a few thousand accessions, for eva- improvement priorities shifted the RHB breeding efforts luation at the Ministry’s Palmira Experiment Station under to the search for sources of resistance to hopperburn, heavy natural virus pressure from 1957 until the epidemic which is controlled by different genes [65]. subsided in 1964 [1]. Natural infection in Palmira revealed In 1967 the Rockefeller Foundation–Ministry of Agri- the high susceptibility (ratings of 7–9) of all tropical indicas culture programme, soon to morph into the newly cre- and most subtropical japonicas. Strong resistance rated as ated International Center for Tropical Agriculture (CIAT), 1–3 was found only in temperate japonicas, largely from began receiving tropical Asian indica germplasm from the Taiwan and Japan, and in a few subtropical japonicas.In International Rice Research Institute (IRRI) located in the subsequent years, other resistant sources, all japonicas, Philippines. This material was evaluated for insect resis- were introduced from West Africa that, in turn, trace tance in greenhouse cages containing a non-viruliferous back to Taiwanese varieties. It is possible that the absence sogata colony. The basic method, which has hardly of RHBV in either northern Asia or West Africa has not changed over time, involved infestation of trays of 15-day- given this neotropical pathogen time to adapt to tem- old seedlings, 10 per accession, with roughly ten indivi- perate japonica rice varieties. Despite the presence of duals (males, females and nymphs) per seedling. Test another tenuivirus, RSV, in temperate Asia, RHBV and materials were rated for damage when the susceptible RSV are antigenically unrelated and their genomes show check, Bluebonnet 50, died some 8–9 days later. Resis- significant differences in nucleotide and amino acid iden- tance to feeding, ranging from moderate to immunity, is tities [43] to expect that resistance to RSV could be conferred by differing combinations of antibiosis, anti- effective against RHBV. In fact, high levels of resistance to xenosis and tolerance. Insect resistance is common in RSV have been identified in indica varieties; and sources of tropical indicas, whereas all Asian temperate japonicas are resistance to RSV, such as Zenith, are highly susceptible to susceptible as are most subtropical japonicas. This is the RHBV [61, 62]. An early study on the varietal reaction of direct opposite of reaction to RHBV wherein all indicas rice to RSV and RHBV had led to the conclusion that rice are susceptible while many japonicas are resistant. CIAT stripe and RHB are caused by different viruses [63]. breeders discard both asymptomatic (extreme antibiosis) Given the significant crop losses caused by RHBV in and highly susceptible materials, preferring only moder- 1956–1958 in Cuba, Venezuela, Panama, Costa Rica and ately resistant reactions having a scale rating of 3–5. Colombia, RHBV resistance breeding began in 1958 using National programmes have released over 300 semi-dwarf several temperature- and photoperiod-insensitive, short- varieties in the American tropics during the past 40 years. grain japonicas from Taiwan as donors in crosses with The great majority are moderately resistant and a few long-grain (USA) subtropical japonicas. Segregating gen- highly antibiotic. There are no confirmed reports of erations were selected under natural RHB incidence, and insect resistance ‘breakdown’ given the emergence of new elite lines were recycled into the crossing programme. sogata biotypes, in contrast to the appearance of suc- RHBV-resistant varieties released in subsequent years, cessive biotypes of the brown planthopper Nilaparvata Napal, ICA10, and Colombia 1, were commercially un- lugens [66] in tropical Asia, presumably caused by the accepted because of poor plant types, low yielding release of monogenic, highly antibiotic resistance. capacity, susceptibility to direct sogata damage and bad A high incidence of RHB in the period 1957–1963, in cooking quality. These defects were not addressed until rice nurseries planted at Palmira, Cauca Valley, Colombia, the introduction of semi-dwarf Asian indicas in 1966– permitted the classification of selected rice varieties into 1967. Colombia 1 and resistant lines derived from crosses four disease reaction groups: (1) a group of RHB-resistant with the new parental materials were used extensively in varieties (Pandhori No. 4, LacrosseC253, Colusa, later years as sources of virus resistance (Peter Jennings, LacrosseZenith-Nira, Gulfrose, Lacrosse and Asahi); (2) 2010, unpublished data). a moderately resistant group (Tainan-iku No. 487, Sadri, Having no acceptable virus-resistant varieties, farmers Missouri R-500 and Arkrose); (3) a moderately suscep- in the early 1960s resorted to insecticides in a futile tible group (Zenith and Century Patna 231); and (4) a attempt to reduce vector populations. The result was group of RHB-susceptible varieties (Toro, Nato, Fortuna, the destruction of biological control and a resurgence of Bluebonnet 50 and Magnolia). These results were fairly

http://www.cabi.org/cabreviews F.J. Morales and P.R. Jennings 7 consistent over a 3 year period, and in different geo- expressed its high level of resistance to RHBV in all of graphic locations in Venezuela, Cuba and Central America these locations [64]. [49]. In Venezuela, a similar RHB evaluation experiment Crop losses to hopperburn and RHB in Cuba, once with 16 rice varieties resulted in the identification of three appreciable, were greatly reduced after the economic disease reaction groups: (1) a highly susceptible group embargo restricted insecticide importations. Rational use (Bluebonnet 50, Starbonnet, NP-125, Nato, Bluebell, of insecticides in most Latin American countries has Zenith, Fortuna, Caloro, Dulor, Century Patna, Kanto 51 gradually diminished feeding damage and RHBV incidence and Saturno); (2) a moderately susceptible group (Var. associated with high sogata populations. These observa- 501 and IR-8; and (3) a resistant group made up by tions suggest that pesticide abuse affects the parasitoids Lacrosse (Colusa-Blue RoseShoemed (R)-Fortuna (R)) and predators of T. orizicolus in rice fields, and that rational and Gulfrose (A Brunimissie selection (R)Zenith) [67]. use of insecticides permits beneficial organisms to effec- These last two rice varieties also behaved as resistant to tively reduce sogata populations. At present, breeders RHB in Colombia. The previous breeding efforts men- place little emphasis on sogata resistance, as most com- tioned above, seeking resistance to RHB, seemed to have mercial varieties and parental materials have acceptable paid off when some new lines, namely ICA-3 and ICA-10, levels of hopper burn resistance. Only elite, advanced proved to be resistant when exposed to field and glass- lines are screened for hopper burn resistance to eliminate house colonies of T. orizicolus under experimental con- susceptible genotypes. CICA 8, an improved variety ditions at Tibaitata, Cundinamarca, Colombia. However, released in 1978 through a joint effort of CIAT, the none of these ICA lines became a variety or was used Colombian Agricultural Institute (ICA) and the Colombian effectively in subsequent breeding programmes. Other National Rice Growers’ Federation (FEDEARROZ), had rice genotypes evaluated as resistant to RHB in that study to be taken out of cultivation during the 1980–1982 included Nilo 3A, ICA3, ICA10, IR 5, Mudgo and Napal. RHBV epidemic, despite its high yielding capacity and Only Mudgo and IR5 were resistant to both the virus and moderate resistance to hopper burn [70]. Fedearroz the vector (hopperburn). The most susceptible genotype, 50, another widely cultivated variety having strong anti- as in previous experiments, was Bluebonnet 50 [68]. This biotic resistance to direct sogata damage, recently suf- susceptible cultivar was widely cultivated in Colombia in fered severe yield losses caused by RHBV in Calabozo, 1957–1958, when RHB caused up to 100% yield losses in Venezuela. The relevant fact is that resistance to the many rice fields. feeding damage caused by sogata does not adequately A number of CICA genotypes possessing high levels of protect against hoja blanca attack in virus-susceptible resistance to sogata feeding damage were developed in varieties, but it seems to reduce RHBV incidence the 1970s. CICA 4 had slight RHBV and good sogata and moderate virus outbreaks under natural field con- resistance [69]. Unfortunately, following its characteristic ditions. cyclical pattern, new outbreaks of RHB in 1981 and 1982 Experiments conducted in the early 1990s [65] showed in Colombia severely affected the CICA lines, particularly that the resistance of rice plants to RHBV was not the CICA 8, widely planted in the eastern plains of Colombia result of differences in vector feeding behaviour. Vectors in 1981 [70]. The main cultivars affected at that time by reared for eight generations on resistant plants showed RHB were IR 22 and CICA 8. The latter genotype is highly no increased ability to transmit to resistant lines or resistant to the direct feeding damage caused by T. orizi- decreased ability to transmit to susceptible ones. The colus, thus demonstrating the need to conduct simul- longevity of vectors was similar when reared on virus- taneous efforts to breed for multiple disease and pest resistant or susceptible plants. The incubation period of resistance, including RHB, planthopper damage and other the virus in resistant plants was significantly longer than in diseases of economic importance, such as rice blast. RHB susceptible plants. Resistance increased with plant age in also affected rice fields in Ecuador, Peru and Venezuela in both resistant and susceptible cultivars. Increased virus the early 1980s, particularly rice cultivars such as CICA 8, dosage, as determined by an increase in the number IR 6, INTI and Araure 1. In response to these RHB out- of viruliferous vectors per inoculated plant, caused an breaks, a special nursery was planted in these countries increase in transmission to both resistant and susceptible to select resistant genotypes. A total of 74 breeding cultivars. However, the ranking of resistant and suscep- lines developed from crosses with selected sources of tible genotypes remained the same across the experi- resistance, namely: Colombia 1, CICA 4, CICA 7, and mental range of dosage and plant age. It was concluded Pelita 1, two RHB resistant controls (ICA 10 and CICA 7) that the resistance studied is to virus infection and there is and three susceptible checks, were included and evaluated little risk of ‘breakdown’ occurring as a result of genetic in this international nursery. RHB incidence was high or behavioural changes in the vector population. The in Ecuador (Guayas) and Peru (Bagua); moderate in authors suggested that these findings would permit the Venezuela (Calabozo); and low in Colombia (La Libertad). application of economic thresholds to planthopper feeding The high disease pressure in Ecuador and Peru affected damage with little risk of RHBV outbreaks. all of the breeding lines and even some of the ‘resis- To study the genetics of resistance to planthopper tant’ controls, particularly CICA 7. However, ICA 10 feeding damage, the more frequently used sources of

http://www.cabi.org/cabreviews 8 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources resistance to hopper burn in Latin America were virus-resistant West African varieties, also products of characterized as resistant or susceptible based on free- crosses with the same Taiwan japonicas, had been incor- choice and no-choice tests and based on the survival and porated into the breeding programme, resulting in addi- oviposition of the insect. Two groups resulted: (1) Mudgo, tional materials carrying RHBV resistance. All these new Amistad 82, IRAT 120, IRAT 124 and Makalioka as parents had been transformed into indica, semi-dwarf, resistant materials and (2) Chianan 8, Colombia 1, Blue- long grain, tropical backgrounds. bonnet 50, IR 8 (ICA), IR 8 (IRRI), Tetep and CICA 8 as The renewed CIAT approach featured the massive susceptible materials. It was found that the damage caused greenhouse multiplication of a highly efficient RHBV vec- by the insect to the materials was associated with insect tor colony for release and infestation of specialized field survival, oviposition and egg hatching. To determine nurseries including several thousand rice parents, lines heritability, two parents were selected: Makalioka and and segregating populations. Vector colony multiplication Mudgo, which were crossed with IR 8. The F1 and F3 in large screened greenhouse cages involved the following populations were also evaluated based on a free-choice key procedures: test. Finally, based on the crosses’ reactions to the insect damage and comparing them with the parents, a genetic 50–60 proven female vectors were mated singly with model of resistance was proposed for Mudgo and Maka- known vector males, establishing 50–60 sub-colonies. lioka, consisting of a single dominant gene in homozygous About 30 nymphs from each mating were individually form (AA), accompanied by a modifier gene that inter- evaluated for virus transmission on individual healthy feres to a greater or lesser degree with the resistance Bluebonnet 50 seedlings. expression (bb>Bb>BB) depending on the material and Surviving insects from sub-colonies having about 90% on the exposure time of the plant to the insect. For transmission were transferred to a large cage contain- Mudgo, the recessive homozygous form (bb) accelerates ing 40–60-day-old diseased Bluebonnet 50 plants grown the expression of the susceptible phenotype, and for in pots. Makalioka the homozygous dominant form (BB) delays the Two insect generations later, a sampling of individual expression of the susceptible phenotype [71]. Lack of insects was tested for virus transmission on healthy proper hopperburn evaluation and classification of some seedlings to estimate the percent colony vectors. of the test genotypes used in this study suggest that Given the labour-intensive crossing and nymph eva- further studies on the genetic nature of hopper burn luation in colony formation, the method was recently resistance are necessary. modified whereby some 2000 field collected insects are From the 1970s to the 1990s, RHB appeared erratically tested individually for virus transmission. Proven vec- throughout the American tropics, although not with the tors are transferred to a large cage for three genera- severity or broad geographic distribution of the 1956– tions of multiplication on diseased rice plants. Percent 1964 epidemic. By then, many new indica varieties resis- colony transmission is estimated from a sample of tant to direct feeding damage but virus susceptible had 100 individuals. replaced the handful of subtropical japonica varieties highly susceptible to both. Some areas such as Bagua in Peru and These modified planthopper colonies typically contain Calabozo in Venezuela became hot spots with moderate about 50–60% RHBV vectors at the time of field release. to high RHB incidence annually. These localized epide- Two colonies are produced each year for two seasonal mics, likely perpetuated by excessive insecticide applica- field screenings. Following the second field trial, remnant tions, facilitated some degree of localized field selection insect stocks are destroyed and the process begins anew against virus susceptibility by breeders. In recent decades, with insects collected from rice farms. Specially prepared no appreciable RHB appeared on the CIAT station, pos- fields contain 50-cm-long rows of plants, separated by sibly influenced by strict pesticide control. Consequently, 10 cm in raised beds 1.1 m wide. Irrigation water is held in CIAT breeders were limited to small-scale evaluation 30-cm-wide canals between beds. RHBV-resistant and of virus resistance in greenhouse tubes and cages, un- -susceptible controls are also included in a randomized satisfactory for a high-volume hoja blanca breeding pro- fashion throughout the beds. gramme. The RHBV resistance derived from Colombia 1 is first Given the slow progress in RHBV resistance breeding expressed when seedlings are about 17 days old. Thus, in the late 1980s, CIAT made a renewed effort based on the evaluation plots are infested with the vector colony induced RHB field epidemics to allow the selection of 18 days after germination. Potted infested plants from the segregating populations. By then, prior greenhouse eva- multiplication cages are gently shaken above the beds until luations had identified several virus-resistant parents, all all nymphs and adults are transferred to the rows of test derived from Colombia 1 and related lines that received seedlings. Vector dosage, difficult to calculate, depends on their resistance from Taiwanese japonicas in crosses made percent transmission within the colony and an estimate in the late 1950s. Oryzica-1 and Metica-1 were two of the of colony vigour. Generally, an average of 1.5–2.0 insects new varieties possessing ‘tolerance’ to RHBV, derived (0.75–1.0 vectors in a 50% transmitting colony) is released from Colombia 1 in the early 1980s [72]. In addition, a few per seedling. After 3 days of infestation, insecticide

http://www.cabi.org/cabreviews F.J. Morales and P.R. Jennings 9 is applied to halt further transmission. Rice lines are active vector of T. orizicolus was p(1)=0.75. This result evaluated 28–30 days later, adequate time for virus incu- means that it only takes one viruliferous sogata per plant bation and symptom expression. to infect 75% of the Bluebonnet 50 plants in a field. On a scale of 1–9 (R–S), the resistant genotype However, when this assay is performed on Colombia 1, a Colombia 1 is usually scored 3–5, occasionally 7. Having source of RHBV resistance, it took six viruliferous sogatas no insect resistance, Colombia 1 is a preferred plant- per plant to induce 75% RHB incidence. This experiment hopper host, which contributes to variability in hoja illustrates various issues treated in this review. First, blanca scores depending on sogata population dynamics, Colombia 1 is neither immune nor highly resistant to that is, the number of viruliferous T. orizicolus individuals RHBV, because if one increases the number of viruliferous that feed on a Colombia 1 plant, plot or field, mainly at the sogatas per plant, disease incidence above 75% would seedling stage. Thus, antixenosis (non-preference) and, to likely occur in Colombia 1. However, even for 75% dis- a lesser extent, antibiosis traits in rice genotypes may ease incidence, each plant of Colombia 1 would have to be influence RHBV incidence in check varieties and test visited by at least 60 individuals of T. orizicolus at an early materials. The highly resistant check, Fedearroz 2000, seedling stage and within a short period of time to induce invariably rates 1–3, while highly susceptible Bluebonnet this level of RHBV incidence in the field, taking into 50 consistently receives a score of 9. As ratings of some account that only about 10% of the sogatas in a given checks are typically variable, all selected materials are population can transmit the virus. This is an unlikely case, evaluated each generation from the F3 to the F6. Materials which explains why the Colombia 1 type of resistance is equal to or better than Colombia 1 are selected, using the effective under field conditions. More important, varieties nearest checks as the basis of comparison. The F1, pro- such as Fedearroz 2000 or some IRAT lines, such as IRAT duced from some 400–500 triple crosses a year, each 124, would theoretically require over 200 sogata indivi- having a minimum of two resistant parents, is handled duals visiting every plant just to reach a threshold of about distinctly. About 20–22 days after infestation, seedlings of 20 viruliferous individuals per plant to cause a RHBV each F1 family are pulled and sorted, discarding all plants incidence of 50% in these genotypes. This is the kind of with any hoja blanca symptoms. Symptomless plants information derived from controlled virus transmission transplanted in the permanent field are destroyed if RHB tests under glasshouse and individual insect cage con- symptoms later appear. ditions that provides rice breeders with an experimental Despite the cost and difficulties inherent in the pro- but fairly reliable vision of varietal behaviour under dif- duction of highly viruliferous vector colonies and in- ferent hypothetical RHBV incidence conditions in the consistent disease ratings in the seedling beds, RHB field. evaluations have been regularly conducted twice yearly Numerous studies on the inheritance of resistance to since the early 1990s. Superior hoja-blanca-resistant plant RHBV have been conducted in the field during epidemics, types with good quality traits are recycled as parents in and in the greenhouse under controlled conditions. The continuing high volume crossing. Most of the current early crossing of RHBV-resistant and -susceptible rice RHBV-resistant rice genotypes selected so far have genotypes suggested that resistance was inherited simply, Colombia 1 in their distant pedigrees, tracing back to probably controlled by a single gene, with resistance Takao-iku 18, a Taiwan japonica, from the 1950s crosses. dominant over susceptibility [74]. In glasshouse experi- Other resistant lines trace to West African IRAT sub- ments, reaction to the virus in the F1 of IR8Mudgo and tropical japonicas that also arose from Taiwanese japo- Bluebonnet 50ICA-10 showed that resistance was nicas, notably Chainan 8. Some lines have both resistance dominant over susceptibility. Segregation in the F2 indi- sources in their parentage. All these parents are now cated that resistance in ICA-10 was governed by two typical long-grain, semi-dwarf indicas. pairs of dominant major genes with complementary action These RHB screening methodologies could be com- [75]. Conclusions from different studies vary from the plemented with more precise biological transmission control by one to two genes, with or without QTLs, and assays based on the probability of infection (p)orno from dominant to partially dominant to recessive action infection (q) of a selected rice genotype by one or more [65, 74–77]. This confusion is attributable to several active vectors of T. orizicolus. This biological assay is based experimental weaknesses including: on a simple binomial formula [p+q=1] and can be per- formed under controlled conditions for promising, Variation in virus readings during natural epidemics advanced lines [73]. Should it be necessary to use more likely because of differing levels of sogata individuals in than one active vector per plant to infect an RHBV- the field, or presence in the host of antixenosis and/or resistant genotype, as is often the case with rice geno- antibiosis against the insect vector. types possessing above average levels of RHBV resistance, Greenhouse cage studies of parents, F1 and segregating the probability of infection of that genotype under field generations are likewise skewed by these components, conditions can be predicted with acceptable accuracy. For principally antixenosis, of resistance to the vector. instance, in previous tests, the probability of infection of Study of individual plants confined in tubes might one plant of the susceptible variety Bluebonnet 50 by one attenuate this variable.

http://www.cabi.org/cabreviews 10 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources Virus dosage effects are an intractable problem in Cultural Practices RHBV transmission and rice germplasm screening studies. Colonies of vectors differ in their ability to The T. orizicolus–RHBV complex is a rice production transmit the virus, and host reaction varies according problem in most neotropical environments where these to the number of viruliferous vectors that feed on a rice planthopper and virus species find warm temperatures, plant. adequate humidity and suitable plant hosts for most of the Seedling age affects disease incidence, with greater year. In tropical America, people preferentially consume susceptibility manifesting in rice genotypes inoculated in long grain, indica rice varieties, which are very susceptible juvenile stages. to RHBV. While significant temperature fluctuations may Host reaction is usually expressed as disease incidence occur in some of these tropical environments, average (number of plants expressing symptoms over total monthly and annual temperatures are always high enough number of plants exposed to vectors) without regard to meet T. orizicolus temperature requirements. Under to disease severity or the existence of possible toler- these general climatic and agricultural conditions, control ance traits in the sensitive host. Greenhouse plants measures directed to the avoidance of the causal agent with traces of infection are considered to be as sus- and the RHB disease are of little value. As mentioned ceptible as killed plants. Such plants in the field would before, RHBV is already widely established in tropical be rated as resistant. America, mainly due to the high mobility of its plant- hopper vector and the propagative nature and vertical The nature of RHBV resistance remains uncertain. transmission of the virus in T. orizicolus. The active inter- Greenhouse and field screening methods conducted at national movement of rice germplasm does not play any CIAT in the early 1990s identified a total of ten possible role in the epidemiology of RHB, other than contributing sources of resistance to RHBV. Genetic analysis indicated to genetic homogeneity in the region, because RHBV is that resistance to RHBV was dominant and controlled by not seed-borne [9]. one gene in cultivar Blue Rose and incompletely dominant RHBV probably has more alternate hosts than those in Takao Iku 18 and PI215936. Resistance was controlled cultivated and wild grasses mentioned above, which might by one gene in Takao Iku 18 and by two independent act as sources of inoculum. However, some of the culti- genes in PI215936 [78]. As mentioned above, the F1 of vated cereals, such as barley, oats and rye, reported as IR8Mudgo and Bluebonnet 50ICA-10 showed that hosts of RHBV, occupy different ecosystems isolated from resistance was dominant over susceptibility. Segregation the traditional rice-growing areas of Latin America, and in the F2 indicated that resistance in ICA-10 was governed the wild grasses suspected of harbouring the virus have by two pairs of dominant major genes with comple- not been shown to be of epidemiological importance. mentary action [75]. Thus, the eradication of grasses suspected of acting as Despite these confounding factors in genetic studies, RHBV reservoirs is not recommended given the long breeders consider RHB resistance to be basically a distance dispersal capacity of T. orizicolus, but it would be dominant trait. Yet, it is a difficult breeding objective interesting to confirm the role of the many grasses that because of the inherent variability of the resistance have been implicated as possible RHBV reservoirs. On the sources available in response to the number of successful contrary, the elimination of volunteer or rattoon rice virus inoculation events (virus dose) per test plant, and plants in rice fields prior to sowing or transplanting of the inconsistencies of the screening methods used. Marker- rice crop is highly recommended. assisted selection is suggested by some breeders as the Rice needs water to produce, either from rainfall or best solution to the expensive and variable field screening. irrigation sources, which satisfies the humidity require- The Latin American Fund for Irrigated Rice (FLAR), ments of T. orizicolus. It is been reported that heavy rainfall located at CIAT, began breeding in 1995, making exten- depresses sogata populations [79], but farmers and sive use of RHBV-resistant parents produced by CIAT. technicians alike have considerable difficulty in evaluating These FLAR crosses resulted in some 30 new varieties population dynamics based on climatic parameters, such released internationally in several tropical countries in as the effect of rainfall, because insect population dyna- 2008–2009. All are rated as resistant to the virus and to mics seldom show synchrony with most climatic pheno- vector feeding. The RHBV resistance generally is equal to mena. Theoretically, planting rice at the onset of the or slightly better than that of Colombia 1. One new rainy season or under irrigation, following a prolonged variety, Fedearroz 2000, has high virus resistance, first dry season without rice or alternate host plantings, manifested in 5-day-old seedlings while moderate resis- should lower the direct or indirect impact of sogata in tance first appears in seedlings after about 17 days. newly planted rice fields. However, studies conducted in Fedearroz 2000 gives consistent field ratings of 1 with an Colombia [20] show that sogata populations are still occasional 3. An indication of the value of this material relatively high prior (January–February) to the onset of comes from Calabozo, Venezuela, a hot spot with an the first rainy season in Colombia (March–April), when endemic hoja blanca situation. The new FLAR varieties upland rice is planted. This is probably a consequence of and lines maintain their resistance in this environment. the residual populations that move from end-of-the-year

http://www.cabi.org/cabreviews F.J. Morales and P.R. Jennings 11 plantings (October rainy season), and the rather short dry affected by an embargo that makes the importation and seasons that characterize the bimodal distribution of rains use of chemical pesticides difficult and infrequent, dem- in Colombia, as opposed to the prolonged dry seasons onstrates the fact that this situation is likely responsible that take place (November–April) in Central America and for the notable reduction in RHBV incidence and sogata the Caribbean. On the other hand, it must be borne in damage in Cuba’s rice fields. On this island, the parasitoid mind that T. orizicolus is very sensitive to dry environ- Paranagrus perforator (Hymenoptera) and the predator ments because of the deleterious effect that low relative Tytthus parviceps (Hemiptera) effect a regular biological humidity can have on egg viability [14]. control of T. orizicolus [80]. Cropping systems have a major influence on the incidence of RHBV. The continuous planting of rice throughout the year in some rice-growing regions creates Chemical Control a permanent source of food and inoculum for T. orizicolus to thrive and act as a virus vector. This situation is further As mentioned above, chemical control has been one of aggravated by the presence of a genetically homogeneous the most widely used methods to control the transmis- crop, usually represented by only one or few cultivars sion of RHBV and hopperburn, despite disappointing grown over a large agro-ecosystem in most rice produc- results in RHBV control with most products used in the tion regions of Latin America and the Caribbean. past [9]. The extensive and intensive use of non-selective, contact insecticides, mainly organo-phosphates and pyre- throids, for sogata control in past decades has been one of Biological Control the main factors responsible for the outbreaks of RHBV and sogata as a pest. However, the RHBV–sogata complex Most pest problems in agriculture are man-made as a is one of the few cases of biological virus transmission for result of the abuse of pesticides. These agrochemicals which a selective systemic insecticide could be effectively often have the most negative impact on non-target bene- used to reduce RHBV incidence, given the circulative and ficial organisms normally feeding on insect pests, such as propagative nature of RHBV inside the sogata vector, sogata. The elimination of beneficial bio-control organisms which takes long enough for a systemic insecticide to kill (parasitoids, predators or entomopathogens) favours the potential vectors. Even active vectors take a few hours to increase of more resistant or mobile insect pest popula- transmit the virus, long enough for a systemic insecticide tion in crops receiving high doses of insecticides or other to kill many viruliferous individuals before they can noxious agro-chemicals. Pesticide abuse is a widespread transmit the virus. The use of selective, systemic insecti- problem in the tropics, where farmers have little technical cides is particularly indicated against viruses transmitted assistance, other than the frequent visits of pesticide in a persistent manner and from within-crop sources, so salespeople, who have an easy task convincing farmers that the insect vectors die before the virus completes that pests, such as T. orizicolus, can result in economically its latency period [81]. Should it be necessary to use a important crop losses if not chemically controlled. The systemic insecticide to control RHBV in highly disturbed main problem with the concept of biological control is agro-ecosystems, it is important to apply the systemic that it does not work effectively in highly disturbed insecticide at sowing time and then every 15 days (chemically contaminated) environments. It takes a con- depending on the degree of RHBV susceptibility of the certed effort on the part of farmers in a given agricultural selected cultivar up to the first month of vegetative area or community to stop abusing pesticides at the same growth. Whereas the cost of these new chemistries is time and for all the crops present. Once a rational pro- relatively high, some of their active ingredients (e.g. gramme of pesticide application has been implemented in imidacloprid) are already available as ‘generic’ products at an agricultural area for some time, biological control a lower cost. But, again, the use of chemicals is a last agents can have a chance to control important pests, such resource to control sogata when large populations of this as sogata. This process is best achieved by rapidly changing planthopper threaten the rice crop as vectors of RHBV or non-selective insecticides by new chemistries (e.g. neo- as direct pests, because even the most selective insecti- nicotinoids and growth regulators) possessing systemic cides available at present have a deleterious effect on and selective action against sucking insects. Among the some important bio-control organisms [82]. bio-control agents known to act against T. orizicolus, there are parasitoids: Haplogonatopus sp. (Hymenoptera), Atrichopogum spp. (Diptera) and Elenchus sp. (Strepsip- Conclusions tera); and predators: Coleomegilla sp. and Cicloneda sp. (Coccinellidae), Zellus sp. (Hemiptera) and several species Undoubtedly, the use of RHBV-resistant rice varieties is of spiders. Entomo-pathogens, such as Beauveria bassiana the best strategy to manage RHB, but the expression of and Metarrhizium anisopliae (fungi), have also been used to RHBV resistance remains ‘dose-dependent’. This means control sogata, but they require high humidity and low that the reaction of an improved rice genotype to the radiation conditions [79]. The case of Cuba, an island virus depends on the number of viruliferous vectors that

http://www.cabi.org/cabreviews 12 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources feed or come into contact with rice plants. Moreover, so that it cannot reach the meristematic tissue, where it RHBV-resistant genotypes may be suffer significant yield can rapidly replicate and then systemically infect the plant. losses if inoculated with RHBV at a very early seedling Alternatively, Fedearroz 2000 may have inherited genetic stage (e.g. 1–3 leaf stage), as was shown for the moder- traits that slow down the cell-to-cell or phloem move- ately resistant rice cultivars Arkrose, Gulfrose and ment of the virus inside infected plants or restrain virus Pandhori No. 4 [83]. RHB is not a unique case in the field multiplication in the plant. of plant virology, regarding the lack of immunity to a virus RHB can be used as a model to study complex virus within the plant species. For instance, this is also the pathosystems. In this system, the traditional ‘disease case of common bean (Phaseolus vulgaris L.) and whitefly- triangle’ of plant pathology: the plant host, the pathogen transmitted viruses (begomoviruses) affecting this crop, and the environment, has to be converted into a ‘disease such as Bean golden mosaic and Bean golden yellow mosaic pentagon’ to include the vector and the environmental viruses, against which no immune common bean genotype conditions that affect its population dynamics. The plant has ever been identified [84]. Nevertheless, acceptable host, rice, continues to be a major staple in the diets of levels of virus resistance can be achieved under natural millions of people in tropical America, and will increase its field conditions in common bean production regions area to meet future demands. Low-yielding upland rice affected by these whitefly-transmitted viruses. Similarly, will continue to be replaced by more profitable irrigated the RHBV screening methods described above permit rice, particularly in Central America, northern Colombia, the discrimination and identification of different levels Bolivia and tropical Brazil. Some traditional irrigated areas of RHBV resistance and subsequent selection of the will decline as water becomes less available, resulting in a most resistant lines to be released as improved rice shift to new production areas having abundant water. cultivars possessing adequate levels of field resistance to Whereas the environmental consequences of changes in RHBV. rice production systems in Latin America are rather The development of rice genotypes possessing high and unpredictable, they might not drastically modify the cur- stable levels of RHBV resistance is possible, as observed rent RHB pathosystem, but they will surely alter the in the case of Fedearroz 2000, a genotype that shows an epidemiology of RHBV. The pathogen itself, RHBV, has unexpectedly high level of RHBV resistance. Crosses not mutated so far, probably because of the fact that the between Fedearroz 2000 and the susceptible line WC 366 few sources of resistance used to date do not confer showed a segregation of resistant, intermediate resistant immunity, so that the pathogen does not need to mutate and susceptible genotypes. The possible genetics of these to survive. This situation could change if new, and as yet observations was a two-gene model with one dominant unknown, genes for RHBV resistance are found and used and one recessive gene or a three-gene model with one by rice breeders. The environmental conditions in tropical dominant and two recessive genes controlling RHBV America will continue to be the same, perhaps somewhat resistance in Fedearroz 2000 [85]. In a biological trans- warmer, which might permit T. orizicolus to expand its mission experiment using two viruliferous sogata indivi- geographic range back into the subtropics. This is oc- duals per (15-day-old) seedling, Fedearroz 2000 showed curring already in the case of northeastern Argentina, only an 8.3% RHBV incidence, as compared with 58% for where T. orizicolus is not only present, but it has been Colombia 1 (a widely used source of RHBV resistance) shown to transmit a different plant virus of maize (Mal del and 100% for the susceptible control Bluebonnet 50. In Rio Cuarto Virus), fortunately under experimental condi- this experiment, the female parent of Fedearroz 2000, tions [86]. According to this report, T. orizicolus survives P 3084/P 3844 showed an RHBV incidence of 66.6%, and in cultivated grasses such as wheat, barley and triticale, the male parent, CT 8154, an intermediate 33.3% virus which are more widely grown in subtropical and tem- incidence. The latter genotype also showed considerable perate regions. While this adaptation to new hosts may plant vigour, and the few infected plants only exhibited not be of epidemiological importance in tropical America, mild RHB symptoms [73]. A molecular study is currently where those cereals are grown mostly in the highlands, it under way to further investigate the genetic traits res- does pose the possibility that T. orizicolus could develop ponsible for the high level of RHBV resistance observed in physiological races better adapted to other grasses dif- Fedearroz 2000. Although this investigation might disclose ferent than rice. Moreover, these cereals (i.e. wheat and the existence of new genes effective against the virus, the barley) have been shown to be RHBV reservoirs [4, 48]. senior author believes that this genotype also possesses On a positive note, the indiscriminate and irrational use of desirable physiological traits derived from CT 8154, which insecticides against sogata is expected to diminish con- might help Fedearroz 2000 escape infection, a known siderably as rice growers become better informed about mechanism of virus avoidance in plants [84]. The fact the negative effects of agro-chemicals on the environ- that RHBV incidence in rice genotypes depends to a large ment, their health and, more important, on biological extent on the age of seedling inoculation shows that the control organisms. This factor, together with the recent plant possesses mechanisms to escape infection. These incorporation of stable RHBV resistance after so many mechanisms may not necessarily be virus-specific, but decades of effort, will likely reduce the incidence of RHB would allow inoculated rice plants to ‘outgrow’ the virus in tropical America.

http://www.cabi.org/cabreviews F.J. Morales and P.R. Jennings 13 RHBV and other tenuiviruses transmitted by plant- and life span. Further studies on the molecular basis hoppers in the Americas (e.g. MspV), Asia (e.g. RSV) and of RHB resistance should result in the selection of rice other continents of the world [87] belong to the same cultivars possessing higher levels of virus resistance. In taxonomic genus (Tenuivirus) but to different phylogenetic the meantime, the implementation of an integrated RHB clusters [43]. RHBV is more closely related to EHBV and management scheme, including: rational use of selective UHBV, two exotic weed tenuiviruses frequently found insecticides; biological control; better cultural practices; in RHB-affected rice fields. These weed tenuiviruses are and use of RHBV-resistant rice varieties, is highly rec- believed to have evolved from an ancestral form of RHBV ommended. [88]. Considering that the above-mentioned tenuiviruses are not seed-borne in their respective plant hosts [40] and that these grass species are not vegetatively propa- References gated, it is possible that the ancestral tenuivirus was dis- seminated to different species of Gramineae by infected 1. Atkins JG, Adair CR. Recent discovery of hoja blanca, a planthopper vectors. It is also possible that the ancestral new rice disease in Florida, and varietal resistance tests tenuivirus could have been an insect virus that eventually in Cuba and Venezuela. Plant Disease Reporter adapted to one of the insect’s plant hosts. This hypothesis 1957;41:911–5. has been considered in relation to the molecular evolu- 2. Garces-Orejuela C, Jennings PR, Skiles RL. Hoja blanca of tion of plant RNA viruses [89, 90], which would help rice and the history of the disease in Colombia. Plant Disease explain the complex interaction between these plant Reporter 1958;42:750–1. viruses, their vectors and plant hosts. Additionally, it 3. Everett TR, Lamey HA. Hoja blanca. In: Maramorosch K, would explain the genetic variability of tenuiviruses and editor. Viruses, Vectors and Vegetation. Interscience, their broad geographic distribution in the absence of seed New York; 1969. p 361–77. transmission. The recent reports of T. orizicolus as a new 4. Morales FJ, Niessen AI. Rice hoja blanca virus. AAB pest of maize in Argentina [47, 86] demonstrate the Descriptions of Plant Viruses. Association of Applied Biologists, Wellesbourne, Warwick, UK; 1985. No. 299: 4 p. capacity of this planthopper to adapt to new hosts and the concern about the potential role of T. orizicolus as a vector 5. Jennings PR, Rosero MJ, Burgos LJ. Hoja blanca del arroz. of plant viruses. Agricultura Tropical 1958;14:511–6. 6. Lamey HA. Varietal resistance to hoja blanca. In: International Rice Research Institute, editor. The Virus Diseases of the Rice Plant 1967. John Hopkins University Press, Baltimore, MD; Summary 1969. p. 293–311.

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http://www.cabi.org/cabreviews 16 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 86. Mattio MF, Cassol A, deRemes AM, Truol 88. Miranda JR, Mun˜oz M, Wu R, Espinoza AM. Phylogenetic G. Tagosodes orizicolus: nuevo vector potencial del placement of a novel tenuivirus from the grass Urochloa Mal de Rio Cuarto virus. Tropical Plant Pathology plantaginea. Virus Genes 2004;22:329–33. 2008;33:237–40. 89. Goldbach RW. Molecular evolution of plant RNA viruses. Annual Review of Phytopathology 1986;24:289–310. 87. Ramirez BC, Haenni AL. Molecular biology of tenuiviruses, a remarkable group of plant viruses. Journal of General 90. Roosinck MJ. Mechanisms of plant virus evolution. Annual Virology 1994;75:467–75. Review of Phytopathology 1997;35:191–209. Author Queries:

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